Abstract Background Gyrodactylus salaris is a directly transmitted ectoparasite that reproduces in situ on its fish host. Wild Norwegian (East Atlantic) salmon stocks are thought to be especially susceptible to the parasite due to lack of co-adaptation, contrary to Baltic salmon stocks. This study i) identifies whether time- and density-dependent mechanisms in gyrodactylid population growth exist in G. salaris-Atlantic salmon interactions and ii) based on differences between Norwegian and Baltic stocks, determines whether the ‘Atlantic susceptible, Baltic resistant’ paradigm holds as an example of local adaptation. Methods A total of 18 datasets of G. salaris population growth on individually isolated Atlantic salmon (12 different stocks) infected with three parasite strains were re-analysed using a Bayesian approach. Datasets included over 2000 observations of 388 individual fish. Results The best fitting model of population growth was time-limited; parasite population growth rate declined consistently from the beginning of infection. We found no evidence of exponential population growth in any dataset. In some stocks, a density dependence in the size of the initial inoculum limited the maximum rate of parasite population growth. There is no evidence to support the hypothesis that all Norwegian and Scottish Atlantic salmon stocks are equally susceptible to G. salaris, while Baltic stocks control and limit infections due to co-evolution. Northern and Western Norwegian as well as the Scottish Shin stocks, support higher initial parasite population growth rates than Baltic, South-eastern Norwegian, or the Scottish Conon stocks, and several Norwegian stocks tested (Akerselva, Altaelva, Lierelva, Numedalslågen), and the Scottish stocks (i.e. Conon, Shin), were able to limit infections after 40–50 days. No significant differences in performance of the three parasite strains (Batnfjordselva, Figga, and Lierelva), or the two parasite mitochondrial haplotypes (A and F) were observed. Conclusions Our study shows a spectrum of growth rates, with some fish of the South-eastern Norwegian stocks sustaining parasite population growth rates overlapping those seen on Baltic Neva and Indalsälv stocks. This observation is inconsistent with the ‘Baltic-resistant, Atlantic-susceptible’ hypothesis, but suggests heterogeneity, perhaps linked to other host resistance genes driven by selection for local disease syndromes.

This study surveys the distribution of Gyrodactylus salaris on resident Arctic charr, Salvelinus alpinus, in lakes connected to three south-Norwegian watercourses: Numedalsvassdraget, Skiensvassdraget and Hallingdalsvassdraget. Gyrodactylus salaris infected charr was only recorded in Numedalsvassdraget. The parasites had the same mitochondrial haplotype as those previously reported on charr in Lake Paalsbufjorden, which is part of Numedalsvassdraget. Since the G. salaris-charr association is persistent in Pa°lsbufjorden and has a wide distribution above the stretches of the watercourse inhabited by anadromous salmonids, this is considered a stable, although perhaps relatively young, host-parasite system. More detailed analyses of these interactions revealed seasonal variations in the parasite population dynamics between late summer and late autumn, with heavier infections occurring in males and older fish in October. This is explained by the combined action of seasonal differences in temperature and physiology and ecology of host cohorts. It is assumed that the occurrence of G. salaris on charr in Paalsbufjorden resulted from a host switch to charr from rainbow trout, Onchorynchus mykiss. Host switches may cause significant expansions of the geographical range of pathogenic variants of G. salaris. Therefore, observations of frequently occurring G. salaris on charr have implications for the diagnosis, management and control of salmonid gyrodactylosis.

Gyrodactylus specimens infecting the skin and fins of two Alpine bullhead (Cottus poecilopus) populations from the rivers Signaldalselva (North Norway) and Rena (South-East Norway) were characterized by both morphological and molecular means. Morphometrical differences were minor and the nucleotide sequences of the internal transcribed spacers (ITS) of the nuclear rDNA cluster were identical for parasites from both localities. Based on earlier descriptions, the relatively closest species are Gyrodactylus hrabei Ergens, 1957, described from common bullhead (Cottus gobio) in Slovakia and G. sp. Malmberg, 1973, from alpine bullhead in Sweden. The Norwegian Gyrodactylus specimens from the two alpine bullhead populations were morphometrically different from both the type material of G. hrabei from Slovakia and newly collected Gyrodactylus specimens from alpine bullhead in two Slovakian localities. The Slovakian Gyrodactylus specimens were found to be identical with type material of G. hrabei. The nucleotide sequences of the ITS of the Norwegian Gyrodactylus species were different from the Slovakian material. Hence, the Norwegian Gyrodactylus specimens from the alpine bullhead represent a new species, G. mariannae sp. nov.

In the present study, we describe the complete mitochondrial (mt) genome of the Atlantic salmon parasite Gyrodactylus salaris, the first for any monogenean species. The circular genome is 14 790 bp in size. All of the 35 genes recognized from other flatworm mitochondrial genomes were identified, and they are transcribed from the same strand. The protein-coding and ribosomal RNA (rRNA) genes share the same gene arrangement as those published previously for neodermatan mt genomes (representing cestodes and digeneans only), and the genome has an overall A+T content of 65%. Three transfer RNA (tRNA) genes overlap with other genes, whereas the secondary structure of 3 tRNA genes lack the DHU arm and 1 tRNA gene lacks the TYC arm. Eighteen regions of non-coding DNA ranging from 4 to 112 bp in length, totalling 278 bp, were identified as well as 2 large non-coding regions (799 bp and 768 bp) that were almost identical to each other. The completion of the mt genome offers the opportunity of defining new molecular markers for studying evolutionary relationships within and among gyrodactylid species.

In recent years, the mitochondrial haplotype diversity of the monogenean ectoparasites Gyrodactylus salaris Malmberg, 1957 on Atlantic salmon and G. thymalli Žitňan, 1960 on grayling has been studied intensively to understand the taxonomy and phylogeography of the two species. According to these studies, neither species can be considered monophyletic, but unfortunately, the geographic sampling has mostly been restricted to Fennoscandia. Only few samples from continental Europe have been analysed, and samples from the United Kingdom have not been included at all. Gyrodactylosis is a notifiable disease in Europe and is in the UK considered the most important exotic disease threat to wild Atlantic salmon populations. In this study, we report six new mitochondrial haplotypes of G. thymalli from England, Poland, and Norway detected by sequencing 745 bp of the cytochrome oxidase I gene. The six new haplotypes add five new clades to a neighbor-joining dendrogram deduced on the basis of the currently known 44 mitochondrial haplotypes for G. thymalli and G. salaris. We conclude that G. thymalli established in the UK along with the immigration of grayling. There is currently no reason to suspect that this parasite is a threat to Atlantic salmon in the UK, although its infectivity to salmon stocks in the UK has not been tested.

The monogenean ectoparasite, Gyrodactylus salaris Malmberg, 1957, has had a devastating effect on wild Atlantic salmon (Salmo salar) since its introduction to Norway in the mid-1970s. In Lake Pålsbufjorden, southern Norway, upstream of the stretches of the River Numedalslågen with anadromous Atlantic salmon, a resident Arctic charr (Salvelinus alpinus) population has been reported to be infected with G. salaris which is viable in the absence of its normal host, the Atlantic salmon. Currently, there is no record of G. salaris infecting Atlantic salmon in the downstream sections of the River Numedalslågen. We studied experimentally the infectivity and reproductive capacity of G. salaris from Lake Pålsbufjorden on wild and hatchery-reared Atlantic salmon as well as on Arctic charr and rainbow trout (Oncorhynchus mykiss). Arctic charr and rainbow trout were moderately susceptible, whereas the Atlantic salmon stocks from River Numedalslågen and River Drammenselva were innately resistant to only slightly susceptible. Thus, the G. salaris from Arctic charr in Lake Pålsbufjorden is considered non-pathogenic to Atlantic salmon. This is the first observation of variation in host preference among Norwegian G. salaris populations. The observed differences in virulence between G. salaris populations could have important consequences for the international legislation and management of Atlantic salmon.

We present the complete mitochondrial (mt) genome of Gyrodactylus thymalli, a monogenean ectoparasite on grayling (Thymallus thymallus). The circular genome is 14788 bp in size and includes all 35 genes recognized from other flatworm mt genomes. The overall A + T content of the mt genome is 62.8%. Twenty regions of non-coding DNA ranging from 1 to 111 bp in length were identified in addition to 2 highly conserved large non-coding regions 799 bp and 767 bp in size. Compared to the recently described mt DNA of the closely related G. salaris from Atlantic salmon from Signaldalselva, Norway, the mitochondrial genome of G. thymalli from Hnilec, Slovakia, differs on average by 2.2%.

Gyrodactylus specimens infecting both anadromous Arctic charr (Salvelinus alpinus) from River Signaldalselva (northern Norway) and resident Arctic charr from Lake Pålsbufjorden (southern Norway) were identified as G. salaris using molecular markers and morphometrics. The infection in Pålsbufjorden represents the first record of a viable G. salaris population infecting a host in the wild in the absence of salmon (Salmo salar). G. salaris on charr from Signaldalselva and Pålsbufjorden bear different mitochondrial haplotypes. While parasites infecting charr in Signaldalselva share the same mitochondrial haplotype as parasites from sympatric Atlantic salmon, G. salaris from charr in Pålsbufjorden bear a haplotype that has previously been found in parasites infecting rainbow trout (Oncorhynchus mykiss) and Atlantic salmon, and an IGS repeat arrangement that is very similar to those observed earlier in parasites infecting rainbow trout. Accordingly, the infection may result from two subsequent host-switches (from salmon via rainbow trout to charr). Morphometric analyses revealed significant differences between G. salaris infecting charr in the two localities, and between those on sympatric charr and salmon within Signaldalselva. These differences may reflect adaptations to a new host species, different environmental conditions, and/or inherited differences between the G. salaris strains. The discovery of G. salaris on populations of both anadromous and resident charr may have severe implications for Atlantic salmon stock-management as charr may represent a reservoir for infection of salmon.

The monogenean Gyrodactylus salaris Malmberg, 1957 is an economically important parasite on Atlantic salmon whereas the morphologically very similar G. thymalli Žitnan, 1960 on grayling is considered harmless. Even molecular markers cannot unambiguously discriminate both species. The nuclear internal transcribed spacer (ITS) sequences are identical in both species, and although mitochondrial cytochrome oxidase I (COI) sequences show substantial variation, no support for monophyly of either species is found. Analysis of nucleotide sequences of the intergenic spacer (IGS) have, however, been interpreted as support for 2 species. Here, IGS and COI sequences from 81 G. salaris and G. thymalli specimens of 39 populations across the species' distribution range were determined. Mitochondrial diversity was not reflected in the nuclear marker. Since various 23 bp IGS repeat types usually differ by just one nucleotide and sequences primarily differ in the number and order of repeat types, alignments may be biased and arbitrary, impeding meaningful phylogenetic analyses. The hypothesis that parasites on rainbow trout represent hybrids of both species is rejected. The presence or absence of particular repeat types is not considered informative. We interpret the IGS data as support for G. salaris and G. thymalli being a single species.

Since the introduction of Gyrodactylus salaris Malmberg into Norwegian salmon rivers in the mid-1970s 46 populations have been infected. Gyrodactylosis caused by G. salaris is a major notifiable disease with a risk of further trans-national spread. The national strategy is to eradicate the parasite by use of rotenone. The strategy has been successful in some small rivers but has failed in all larger infected river systems. Alternative strategies are thus clearly needed. Genetic selection for increased resistance to G. salaris has not been investigated until now. We estimated additive genetic variation and heritability of survival in a pedigreed family material of Atlantic salmon parr subjected to a controlled challenge test with G. salaris. To obtain the family material eggs were fertilized in a hierarchic mating design to produce 49 full-sib groups of salmon within 25 paternal half-sib groups. When reaching an average size of 8 g progeny (n = 973) were challenged with G. salaris and the test was run until mortalities stopped. Dead fish were removed daily and together with the survivors, DNA fingerprinted for family identification. Mortalities started after ca. 15 days, peaked at around day 45 at a level of ca. 50 individuals, declined sharply and leveled out close to zero. Only 11.3 % of the 973 salmon survived the test, but the course of mortality varied significantly between full-sib families. In eleven of the 49 full-sib families all fish died, whereas the 4 least affected families had survival rates between 36-48%. Estimated heritability of survival (on the liability scale) was 0.32 ± 0.10. Time until death and the ability to survive were not expressions of the same genetic trait. Selecting survivors as parents for the next generation for restocking is expected to improve the overall survival rate significantly and can be used as a disease control measure to contain the infection at a level where the parasite ceases to be a major problem.

In the course of the presented study 413 grayling (Thymallus thymallus) and 89 brown trout (Salmo trutta) were collected from 29 localities belonging to 15 Austrian watercourses, all within the Danube drainage system, and investigated for infection with monogenean Gyrodactylus. A total of 41 grayling (9.9 %) and 80 brown trout (89.9%) showed an infection. Sequencing of the internal transcribed spacer (ITS) regions 1 and 2 of the nuclear ribosomal DNA (rDNA) cluster was used for species identification of 92 collected Gyrodactylus specimens. Three species were detected; of the 49 parasites from grayling 32 were identified as G. thymalli/G. salaris (65.3%), 11 as G. truttae (22.5%), and 6 as G. teuchis (12.2%). Of the 43 Gyrodactylus individuals sampled from brown trout 3 turned out as G. thymalli/G. salaris (7%), 25 as G. truttae (60.5%), and 13 as G. teuchis (32.5%). Trout infections frequently exceeded 30 Gyrodactylus specimens per fish, whereas for grayling there was a maximum of 3 parasite individuals per fish. In several cases, a host population of a particular sampling locality was infected with different Gyrodactylus species, whereas mixed infections of particular host individuals were rarely observed. For 35 G. thymalli specimens 745 bp long sequences of the mitochondrial cytochrome oxidase subunit 1 (COI) gene were determined. These sequences represented 10 new haplotypes that group into at least 2 well supported clades in phylogenetic analyses using all currently known mitochondrial haplotypes of G. thymalli/G. salaris. The two new clades show average K2P distances of 0.01-0.031 to all other previously described clades. None of the 4 different phylogenetic approaches, i.e. Neighbor-joining, Maximum, parsimony, Maximum likelihood, and Bayesian inference, could resolve the basal internal nodes with high statistical support. Thus, the G. thymalli parasites from the Danube included in the current study do not provide support for the hypothesis that the Danube basin served as a glacial refugium for Northern European G. thymalli/salaris.

A number of biologists have independently gathered together and made publicly available, information relating to the monogenean genera known in their time. Of these, Yamaguti’s Systema Helminthum, produced over 40 years ago, remains the first point of reference for many helminth researchers. In terms of existing web-based resources, whilst there are a number of sites specialising in particular genera or regional fauna, there are very few that have tried to synthesise current knowledge concerning the Monogenea. Given the lack of such a synthesis, basic taxonomic and biological information concerning the numerous known monogenean genera is frequently difficult or impossible to access, often being published in grey literature or inaccessible journals, which may be beyond the reach of researchers with limited budgets or informational resources. Even when such data are available, images and descriptions of taxonomically informative traits are of variable quality. This paper describes the development of a web-based resource, the steroid enhanced big sister of “GyroDb”. We have started to construct a web site, the eponymously named “MonoDb”, which will provide access to records for recognised (and retired?) monogenean genera. In addition to overviews of monogenean biology, taxonomy and relevant research techniques written by acknowledged experts (any takers?), access will be provided to individual species records arranged by family and genus. Each species record will comprise images and molecular data relevant to their taxonomic identification, original references for descriptions and other key information e.g. host and habitat etc. For type species and other important species or species groups, the site will contain authored reviews of current biological and systematic knowledge. In the future we intend the site to allow users to submit new data which will be refereed to ensure quality and consistency before upload to the publicly accessible databases. It is intended that the site be accessible for users of all backgrounds and interests including both those with a casual interest in monogeneans and established researchers. Links to relevant sites such as FishBase and researcher and facility homepages will also be provided. A provisional version of MonoDb may be accessed at www.MonoDb.net.

Anadromous Arctic charr (Salvelinus alpinus) and sympatric Atlantic salmon (Salmo salar) have both been found infected with G. salaris in some river systems in North Norway. In the present study we explore the potential of resident Arctic charr as host and reservoir for G. salaris in the absence of Atlantic salmon. Arctic charr were sampled with gill nets in nine lakes from four water currents in southern Norway, fixed in ethanol and screened for Gyrodactylus under a stereomicroscope. Gyrodactylus were found on Arctic charr in five lakes. In four of these lakes (upstream the anadromous stretches of Numedalsvassdraget) G. salaris was identified by means of both molecular markers and morphology. The infection has persisted through years (2000-2005) in at least one of these localities (Lake Pålsbufjorden). This locality was sampled in August and on the spawning grounds in October 2005. Both prevalence and abundance of Gyrodactylus was highest in October. In addition, prevalence, abundance and mean intensity of parasites was higher in males than in females. A more detailed study of the distribution of G. salaris in Arctic charr cohorts (2-7 year) in October revealed a positive correlation between age and prevalence. The finding of G. salaris in four lakes, and the persistence and relative high levels of the infection in Pålsbufjorden, indicates that Arctic charr is able to sustain an infection without sympatric Atlantic salmon.

One of the most important flatworms to have successfully colonized new fish populations is the monogenean Gyrodactylus salaris infecting Atlantic salmon (Salmo salar) and rainbow trout (Oncorhynchus mykiss). This ectoparasite has devastated wild salmon populations in Norwegian river systems since its introduction from the Baltic area in the mid-70ies. In some north Norwegian salmon rivers, co-occurring anadromous Arctic charr (Salvelinus alpinus) populations are also infected with G. salaris. A parasitological examination of a resident Arctic charr population in Lake Pålsbufjorden (Buskerud County, south Norway) draining into the commercially important salmon river Numedalslågen, have revealed a persistent G. salaris infection with a mtDNA haplotype identical to the virulent River Drammenselva strain. The lake is situated ca. 50 km upstream of the nearest Atlantic salmon river system where G. salaris has never been reported. This is the first observation of G. salaris maintaining a viable population in the absence of other salmonid species known to be susceptible for G. salaris. A persistent G. salaris strain on Arctic charr without infecting Atlantic salmon in the same river system raises the question whether or not this particular strain can still infect Atlantic salmon. This initiated an experimental study on the infectivity and reproductivity of the G. salaris strain from Arctic charr on the same host species in addition to Atlantic salmon and rainbow trout. Each fish were infected with one G. salaris experimentally transferred from the Arctic charr, and individually isolated. Concurrently, G. salaris of the same haplotype but from Atlantic salmon, was used as a control. The results demonstrated that Arctic charr and rainbow trout were moderately susceptible and responded, whereas the Atlantic salmon stock from River Drammenselva appeared almost resistant. This is the first observation of differences in reproductivity (i.e. virulence) between G. salaris strains of the same mtCO1 haplotype.

Economically, one of the most important platyhelminths to have successfully invaded novel fish populations is Gyrodactylus salaris. This ectoparasitic monogenean has devastated stocks of wild Atlantic salmon in Norway since its introduction from the Baltic during the 1970s. The parasite with its high fecundity and transmission potential can rapidly colonize an entire river system. Having no specific transmission stage, G. salaris utilizes four different routes of transfer to new hosts: via contact with live hosts, via dead hosts, by detached parasites drifting in the water column, and by parasites attached to the substrate. However, the relative importance of these different routes is largely unknown. In the current study, we evaluate the transmission strategies of G. salaris focusing on the importance of dead hosts, by assessing the survival and infectivity of detached worms and those removed from dead hosts. At 18oC, survival off the host is 1d, but at 3oC parasites survive for 4d. Surprisingly, however, most parasites remain with their host following its death. Such worms survive despite being wrapped in decaying host tissue, their life span being doubled compared with individuals maintained in vitro, probably sustained by feeding on the dead host. G. salaris can actually survive for up to 6d at 12oC on a dead host and, importantly, are still infectious, at least up until 72h post-host death. This survival strategy is in stark contrast to that previously observed for individuals of G. turnbulli in which parasites actively leave a dead host. For G. salaris, dead hosts may serve as an important infection source. In these experiments, worms were also aged to determine whether transmission was influenced by life span. It appears that worms that have given birth are more likely to transfer to a new host than those that have not given birth. Thus, although having no specific transmission stage, gyrodactylids apparently do display a non-random timing of transmission. The present results highlight the importance of dead hosts as a significant reservoir of infection. Taken the significant threat that G. salaris constitutes to populations of Atlantic salmon, this is an aspect which should be incorporated into future management polices and risk assessments. This work was supported by the National Centre for Biosystematics (Project no. 146515/420), co-funded by the NRC and the NHM, University of Oslo, the NRC Wild Salmon Program (Project no. 145861/720) and a Natural Environment Research Council Advanced Research Fellowship (NER/J/S/2002/00706).